Visitation patterns of endangered grey parrots (Psittacus erithacus) in a forest clearing in the Democratic Republic of the Congo

Abstract The grey parrot (Psittacus erithacus), once abundant, has become increasingly threatened due to the combined effects of capture for the global pet trade and habitat loss. Although grey parrots are well studied in captivity, effective conservation efforts require a better understanding of their ecological requirements in the wild. The aim of this paper is to quantify grey parrot behaviours across the annual cycle. To do that, we studied groups of grey parrots gathering in a natural forest clearing in the Nkuba Conservation Area, eastern Democratic Republic of the Congo. Using parrot counts and focal sampling, combined with descriptive statistics, we found that an average of 40 grey parrots visited the clearing each day, following a regular pattern in which they first perched in the trees surrounding the clearing, vocalizing loudly, until the group landed in the clearing to feed, drink and interact with each other. Generalized linear models (GLMs) and generalized additive models (GAMs) showed that the time at which parrots arrived, landed at, and left clearings was influenced by the weather, seasonality and the month of the year. We also found that parrots shortened their visits when disturbed by predators or the presence of humans. Although the underlying mechanisms for grey parrot visits to forest clearings remains unclear, the consistency of this behaviour observed elsewhere in Africa and the feeding observed in the clearing in this study suggest that these area support important foraging habitat for the wild grey parrots. Therefore, ensuring the availability of such clearings is paramount to the long‐term survival of the species. We suggest that future efforts to protect grey parrots in their native habitats focus on identifying clearings visited by parrots, monitoring these clearings and allowing parrots to visit them without disturbance or risk of capture.


| INTRODUC TI ON
The endangered grey parrot (Psittacus Erithacus) is a once-abundant keystone species (Blanco et al., 2018) in its 5-million-hectare range throughout west and central Africa (BirdLife International, 2022;IUCN, 2023).Most previous studies on wild grey parrots have examined their habitat-use, their diet and threats to the species in its African range (Amuno et al., 2007;Annorbah et al., 2015;Chapman et al., 1993;Chupezi et al., 2006;Dueker et al., 2020;Hart et al., 2016;Marsden et al., 2016;May, 2001;Piebeng et al., 2018;Tamungang & Ajayi, 2003;Tamungang et al., 2014Tamungang et al., , 2016)).These studies have mainly found that wild grey parrots inhabit both primary and secondary rainforests where they feed on a large array of plant parts such as seeds, fruits, leaves and buds.Grey parrots roost in groups and their breeding season lasts from March to November when they raise an average of two chicks in tree cavities.Grey parrots are prey to several animal species such as cats and raptors.
Unfortunately, grey parrot populations underwent rapid declines in the last decades (50-79%, IUCN, 2023) due to a combination of factors including capture for the pet trade (Annorbah et al., 2015;Marsden et al., 2016;Martin, 2018) and deforestation (Hart, 2013;IUCN, 2023;Martin et al., 2014).Although these declines have drawn the attention of the conservation community (Amuno et al., 2010;Annorbah et al., 2015;Chapman et al., 1993), few studies have attempted to close the knowledge gap on behaviours of grey parrots in the wild (Bentley, 1999;Hart, 2013;May, 1996), although such knowledge is crucial for the protection of the species, and a priority for future research (Martin et al., 2014).
It is challenging to study wild grey parrots as they live in remote forests, travel daily across large distances and are difficult to observe while feeding in high canopies (Amuno et al., 2007;Chapman et al., 1993;Marsden et al., 2016;Martin et al., 2014).Instead, grey parrots may be studied at communal roosts, at drinking sites or when visiting natural forest clearings characterized by marshy or muddy soil (Martin et al., 2014;Tamungang et al., 2014).Such clearingsalso referred to as salt/clay/mineral clearings/licks-attract large numbers of parrots and are likely to play a key role in parrot ecology as they contain minerals important for the parrots' diet (Chupezi et al., 2006;Hart, 2013;Martin et al., 2014).Geophagy is common among parrots (Burger & Gochfeld, 2003) and is often reported in South America where various Neotropical parrots visit clay licks to ingest clay and supplement or detoxify their diet (Brightsmith & Villalobos, 2011;Burger & Gochfeld, 2003).Unfortunately, because these clearings attract large flocks of grey parrots that are vulnerable when foraging on the ground, they are sought after hunting grounds for poachers (Hart, 2013).
Forest clearings visited by parrots are likely scarce in the Congo basin (Hart, 2013) and few such clearings have been reported in literature (Table 1).In each case, flocks of hundreds of grey parrots were seen foraging and drinking on the ground.Studies on the behaviour of grey parrots in clearings in Lobéké and Dzanga NP (Bentley, 1999;May, 1996May, , 2001)), carried out from a hide every morning, showed that parrots started gathering in the trees surrounding the clearing an hour after dawn, after which the first parrots descended into the swamp to forage on plants and soil (Bentley, 1999).As the reported observations were limited to a single season (dry season in May, 1996 andBentley, 1999) or even single observations (Hart, 2013), there is so far no knowledge on how parrots use clearings throughout the year.
Yet, several factors may influence the visitation patterns of the clearings by grey parrots, including rainfall seasonality.Wet and dry seasons are characterized by marked differences in food availability within the forest, especially a lower amount of fruits during the dry season (Adamescu et al., 2018;Tamungang & Ajayi, 2003;Van Der Hoek et al., 2021), and would therefore influence how much parrots would rely on the resources found in the clearing.The breeding season of the parrots, which lasts from March to November, may also impact the use of clearings by parrots as they provision young (mainly during the dry season of June-September, Piebeng et al., 2018).
Studies carried out in licks in the Amazon indeed show that parrots visit licks most often during the breeding season when they need additional nutrients (Brightsmith et al., 2018).Finally, potential disturbances, like the presence of predators or humans, could cause the parrots to leave the area earlier than expected (May, 1996).Given the importance of clearings for the grey parrot and the significant threat of poaching, more information on visitation patterns throughout the year is urgently needed.

TA B L E 1
Overview of studies on grey parrots in salt licks in chronological order.Here, we report the visitation patterns of grey parrots in a clearing in the easternmost part of their range: the Nkuba Conservation Area (NCA) in eastern Democratic Republic of the Congo (DRC).The aim of our study is to quantify grey parrot behaviours across the annual cycle as they visit the clearing.We first tested whether visitation timings (arrival, landing and departure times), visit duration, visitation rate (presence and absence of the parrots) and the group size of the parrots are consistent throughout the year or varies among seasons, as food availability in the forest can vary between the wet and the dry season, and therefore, influence the visitation patterns and the number of parrots in the clearing.Second, we tested whether morning weather, which was shown to affect visitation patterns of parrots in licks in South America (Brightsmith, 2004), influenced visitation patterns and group size.Third, since the occurrence of disturbances could influence departure time and visit duration, we included disturbance in the model for those two response variables.
Second, we tested whether activities of the parrots in the clearing (feeding, drinking, preening, interacting, moving around the clearing or mating) differed between seasons as the need for food or water from the clearing or the occurrence of mating activities may be dependent on the time of the year.Lastly, we discuss the implications of our findings for conservation actions.

| Study site
The focal forest clearing is found in the Nkuba Conservation Area (hereafter NCA; 1°17′ S, 27°31′ E; ~500-1500 m.a.s.l.), a ~2460 km 2large community reserve located in the North Kivu and Maniema Provinces, DRC.The NCA is located between Maiko and Kahuzi-Biega NP (Figure 1).The area is covered by lowland rainforest and has a tropical climate with average annual temperatures of 24.2°C and precipitation between 2100 and 2500 mm yr −1 , with peaks during two wet seasons from April to May and September to December (Karger et al., 2017)  when all parrots had departed from the area, which was recorded as the 'departure time'.These times were subsequently transposed to minutes after sunrise to account for variation in day length throughout the year (See Table A2 for sunrise hours in the study area).
From these, we calculated two additional metrics: the 'presence/ absence' of the parrots on any given observation day in the clearing as whether they landed on the ground of the clearing (presence) or not (absence) and the 'visit duration' as the amount of time between the landing of the first parrot and the departure of the last parrot from the clearing.
We determined the daily 'group size', which we considered as the maximum number of parrots that landed in the clearing during an observation session.Group size was determined based on the counts of the number of parrots present in the group located inside the clearing performed every 10 min from landing time to departure time.It was impossible for the observers to evaluate how many parrots were perched in the trees from their observation point situated inside the forest, and we must therefore use the maximum number of landed parrots as a proxy for the total group size for each session.
In between these counts, the observers performed focal sampling of the behaviour of individual parrots (Martin & Bateson, 2007).Based on the focal sampling data, we calculated the percentage of time focal animals spent on predefined behaviours.In focal sampling, the duration of all the behaviours (moving, drinking, feeding, mating, preening or interacting) of a randomly selected parrot was continuously recorded over the course of 5 min or until the individual was out of sight.If the focal individual was out of sight within the first 2 min of the sampling, the observers selected another individual.They followed this bird for 5 min or until this individual was out of sight, until the next parrot count.Note that, when parrots were foraging on food items on the ground, it was impossible for the observers to identify with certainty whether they fed on soil or plants.Even when parrots pulled plants out of the ground to consume them, observers were unable to distinguish which part of the plant or which species of plant was consumed.
In addition to visitation data or patterns, we recorded environmental variables that would be relevant to explain visitation patterns.First, the observers recorded three types of disturbanceshuman noises, the presence of raptors, and alarm calls emitted by great blue turacos (Corythaeola cristata) -as these could scare off the parrots and influence the departure time and therefore the duration of their stay (May, 1996).Second, we registered whether it rained in the morning during the observations (morning weather) as rain was shown to influence visitation rates of parrots in licks in Peru (Brightsmith, 2004).Third, observation dates were classified into V falls between 0 and 1 (where 0 indicates no association and 1 would indicate a perfect association).We considered a value of >0.15 to be a strong association (Akoglu, 2018) and refrained from using explanatory variables in the same model if their Cramer's V was above the 0.15 threshold.We found no significant correlation between season and disturbance (X 2 p-value = .02).Morning weather was moderately correlated to both season (there are more rainy mornings during the wet season, X 2 p-value = .12and Cramer V = 0.12) and disturbances (there are less disturbances on rainy mornings X 2 p-value = .38and Cramer V = 0.13).Group size was strongly correlated to all three environmental variables (Season X 2 p-value = .65and Cramer V = 0.66, Morning weather X 2 p-value = .50and Cramer V = 0.50 and Disturbances X 2 p-value = .1 and Cramer V = 0.78).We therefore did not use group size as an explanatory variable.

| Statistical analyses
We first described the visitation patterns of daily visits by report- <.001), we added the median and 1st and 3rd quartiles.Because daily activities of the parrots may be affected by seasonal food or water availability, we tested whether the time spent on behavioural activities during a given visit varied between dry and wet seasons using linear models from the stats package (R Core Team, 2022).We then fitted generalized linear models (GLMs), which do not assume data normality, to determine whether season (wet or dry) or morning weather influenced any of the response variables (visit duration, arrival time, landing time, departure time, presence/absence and group size), and whether disturbance influenced departure time and visit duration.We used the glm function of the 'stats' package in R (R Core Team, 2022) with Gaussian or logistic (for presence/absence) distributions.We considered pvalues of less than .05significant.We consider models with R 2 values of at least .1 to be biologically meaningful while results from models with R 2 smaller than .1 should be interpreted with caution (Chalmer, 1987).
Apart from differences among seasons, we looked for 'within-

| RE SULTS
We found that grey parrots have a consistent pattern of visitation with distinct arrival, landing and departure times (Figure 3).).We found that there were on average 39.4 parrots (SD = 28.2) on the ground at any given time, though we recorded groups of up to 155 individuals.We recorded 805 focal samples, spanning a total of 57.9 h, from which we derived that grey parrots spent most of their time feeding (62%), interacting with each other (15%) and moving around (15%).They spent smaller portions of their time (<3%) drinking, preening or mating (Figure 4).
Generalized linear models revealed that during the wet season, parrots landed later (p = .001,R 2 = .2,see all results of the GLMs in Table 2), and remained for a shorter period of time (p = .003,R 2 = .2),than during the dry season.They also spent a significantly larger portion of time drinking water during the wet seasons (2.5% and 15.2% of time during the dry and wet seasons, respectively, p = .005,R 2 = .06,Figure 4).There were no significant differences between seasons in the proportion of time spent on other behaviours.
Additionally, we found that parrots, which landed in the clearing 77 of 100 days of observation, were more likely to land in the clearing on dry mornings rather than on rainy mornings (p < .001, 2) and that on dry mornings, they arrived earlier (p = .05and R 2 = .05),landed earlier (p = .02,R 2 = .2) and stayed longer (p = .01,R 2 = .2).We also found that parrots landed in larger groups during the dry season (p = .004and R 2 = .2) and on dry mornings (p = .004and R 2 = .2). Finally, we found that parrots visited clearings for shorter periods of time (p = .001,R 2 = .2) on days with at least one disturbance.
Monthly visitation patterns corroborated our observations of seasonal patterns in clearing visitation and revealed additional, significant fluctuations for visit duration, arrival time, landing and departure time, presence/absence and group size (GAMs: p < .05for all; Table 2, Figure 5).We found that daily visits were especially long in the July (dry season) and short over the September-December

| DISCUSS ION
Our study is the first to quantify the timing of grey parrot behaviours across their annual cycle.Our observations in Ungwe confirm that the clearing is heavily used by wild grey parrots throughout the year, that they visit the clearing on a near-daily basis and that these visits occur after sunrise and end before noon.Additionally, we observed that when visiting these clearings, parrots followed a pattern consistent to those described in Bentley (1999) and May (1996): Soon after dawn, parrots gather and vocalize in the trees near the clearing.
Landing occurs roughly an hour later.Grey parrots mainly feed, interact and drink at the clearing for about another hour, or until there are disturbances (e.g.human noises, presence of raptors or alarm calls emitted by the Greater Blue Turacos).Such consistent patterns and the high frequencies of the visits suggest that visitation of clearings constitutes an important component of the daily routine of the parrots and plays a key role in the ecology of these endangered birds.
We observed that grey parrots spent most of their time feeding in the clearing, supporting previous observations of similar behaviours and indicating that these clearings constitute an important food source for the species (Bentley, 1999).While grey parrots are mostly known to feed on buds, flowers, seeds and fruits of trees (Tamungang & Ajayi, 2003), we corroborate findings that they also consume ground plants when visiting waterlogged clearings (Bentley, 1999).
Although we were unable to detect geophagy during our observations, grey parrots may ingest specific minerals via the consumption of (muddy) water or ground plants present in the area.Future research should focus on studying the seasonal vegetation composition and testing the composition of the water and the soil of the clearing.
Additional studies on the diet of wild grey parrots might also be required to determine the exact reasons behind clearing visits.
Even though they were rather consistent, visitation patterns of the clearing fluctuated throughout the year, with peaks in the likelihood, duration and number of parrots visiting during the dry months TA B L E 2 Output of explanatory models for patterns in the arrival time, landing time, departure time, visit duration, presence/absence and group size of grey parrots visiting clearings in the Nkuba conservation area, with significant effects in bold..004

Model
Note: Generalized additive models (GAM), with months with highest/lowest predicted values, for arrival, landing and departure times this implies the latest/earliest times (in minutes after sunrise), respectively; Generalized linear models (GLM).Boxes in grey represent untested combinations of variables.
of July and August.The larger groups we observed during the dry seasons could be driven by the need for additional food resources and/or detoxifying agents necessary to supplement a poorer and more toxic diet caused by scarcity of food in the forest (Adamescu et al., 2018;Tamungang & Ajayi, 2003;Van Der Hoek et al., 2021).
This also explains why the clearing was particularly attractive to parrots during the dry months of July and August, during the beginning of the chick-rearing period when all available food sources must be exploited (Brightsmith et al., 2018).Yet, the main predictor of the presence of parrots in the clearing across the year was rainfall, with parrots landing less often in the clearing when it rained.Rain is indeed associated with diminished bird activity and was shown to prevent parrots from visiting licks in Peru (Brightsmith, 2004).
We also found that during the dry season, when flocks are bigger, parrots landed and stayed longer, a pattern possibly linked to anti-predator defence behaviour (Burger & Gochfeld, 2003).Main predators of grey parrots are large cats, raptors (e.g.goshawks regularly observed flying in the clearing, Table A1), and humans (Piebeng et al., 2018), to which Grey parrots are particularly vulnerable when they feed on the treeless ground of the clearing.Larger flocks are thus better protected against these threats as it allows the group to have more individuals watching out for predators while parrots are feeding (Westcott et al., 1988) and large flocks taking off together tend to confuse predators, diminishing the risk for a successful attack (Landeau & Terborgh, 1986).When parrots were disturbed and took off, they generally all left the area and did not return to the clearing, which is consistent with findings from Dzangha NP (May, 1996).
Unfortunately, we were unable to visit the clearing during the short rainy season of April to May.This can impact our results as we may have missed some temporal variations within the annual cycle, especially since this period corresponds to the beginning of the breeding season of the parrots, when they court each other, search for nests in tree cavities and lay eggs (Piebeng et al., 2018).It is diffi- In Ungwe, we observed groups of up to 155 parrots visiting the clearings, though this is an underestimation of the total number of parrots in the area as we could only count the parrots present on the ground (Bentley, 1999).Nevertheless, considering the spectacular groups of hundreds of parrots reported to visit the Lomami NP located a few hundred kilometres from the NCA (Hart, 2013), groups of over 800 individuals in Cameroon (Bentley, 1999), and roosting sites with 700-3000 grey parrots in Ghana (Annorbah et al., 2015), we may interpret our numbers as relatively low.Since there are natural local variations in food availability and in the densities of parrots within their range (Marsden et al., 2016), it is possible that the small group size we observed is in line with historical numbers in the area.
However, capture for the pet trade recently occurred -and may still be occurring -in and near the NCA (Personal observations), so grey parrots in this region may have experienced declines due to harvesting for the pet trade (Hart, 2013;Hart et al., 2016).
While our research shows the importance of the Ungwe clearing as a food source for grey parrots across an annual cycle, there may

2. 2 |
Data collectionBetween July 2021 and July 2022, two trained observers, including B.I., visited Ungwe for nine periods of 7-12 consecutive days spread over the year and across seasons (for a total of 276 h of observation across 100 days).However, due to logistical constraints (lack of available trained observers and access to the clearing made difficult by the heavy rains), we were unable to visit the clearing during the short rainy season of April to May and during the month of September.Each observation session started at approximately 6 a.m.before the parrots had arrived in the area and ended before noon when all parrots had left the area.During this time, observers stayed concealed in trees surrounding the clearing.To answer the abovementioned research questions, we collected five types of information on the parrots' visits to the clearing: timings, group size, behaviour, disturbances and environmental variables.Observers recorded the 'arrival time', the time at which the first parrot perched in trees adjacent to the clearing, often detected as they vocalized, and the 'landing time', the time at which the first parrot landed on the ground in the clearing.The session ended wet and dry season based on the month (i.e.wet from April to May and September to December).We ran Pearson's Chi-squared tests between morning weather, season, disturbance and group size to see if they were correlated and evaluated the strength of the relationship of correlated variables using a Cramer-V test, using the 'tidyverse' and 'lsr' packages in R(Navarro, 2015; R Core Team, 2022;Wickham et al., 2019).Cramer's ing the maximum, minimum, mean and standard deviation (SD) of arrival time, landing time, departure time and visit duration.As arrival time was not normally distributed (Shapiro test, p-value F I G U R E 1 The Nkuba conservation area (NCA) located South of Maniema National Park and North of the Kahuzi-Biega National Park in eastern Democratic Republic of the Congo.In red is the location of the Ungwe clearing.F I G U R E 2 Picture of a flock of grey parrots visiting the Ungwe clearing in the Nkuba conservation area in Democratic Republic of Congo (author C. Fastré).
season' fluctuations in visitation patterns by determining for which month visitation patterns and group size were lowest and highest.While fully acknowledging the limitations of our data (e.g.we lacked data for September, March, April, and May), we also fitted generalized additive models (GAMs) with months fitted along a smoothing spline (knots = 9) as a predictor variable for presence/absence of parrots (binomial), visit duration, group size, arrival, landing and departure times (all Gaussian).Given the scarcity of our data overall as we lacked data from 4 months, and the even more limited number of observations of specific activities (e.g.drinking), we opted not to use GAMs to examine temporal patterns in observed behaviours.We used R packages 'mgcv'(Wood & Wood, 2015) and 'MASS'(Ripley et al., 2013) to fit these models and derived fitted values using the 'itsadug' package(van Rij et al., 2020).All statistics were performed in R (R Core Team, 2022).

F
Arrival, landing and leaving times of grey parrots visiting a forest clearing in the Nkuba conservation area in the Democratic Republic of the Congo (in minutes after sunrise).The width of the violin plots shows the number of observations for each time after sunrise.The boxplot shows the median, first and third quartile.F I G U R E 4 Proportion of time (%) spent by grey parrots at a forest clearing in the Nkuba conservation area in the Democratic Republic of the Congo during dry season, wet season and averaged over the entire year of the study (Year, July 2021-2022).
wet season-lack of data does not allow us to confirm if this pattern also holds for the April-May wet season-a result of early arrival and landing times and late departure times in July, and relatively later arrival and landing times in other months (February and December in particular).Similarly, the likelihood of parrots visiting on a given day (presence/absence) and group size peaked during the dry season months of July and August and were reduced over the September-December wet season.
cult to know whether parrots would vary their visitation patterns of the clearing during this period.While our data during the wet season of October to December show that parrots are less likely to visit the clearing on rainy mornings, which occur more often during the rainy season, our results also suggest that parrots visit the clearing more often in July and August, during the peak of the breeding season.It is therefore important that future research focuses on gathering more data on the use of clearings during the beginning of the breeding season.More observations during this period, during which parrots court each other and mate, might also increase the number of mating activities observed in the clearing, since parrots do not mate near their nests(Piebeng et al., 2018).

F
Examples of temporal (monthly) patterns in grey parrot visits of forest clearings in the Nkuba conservation area as observed between July 2021 and July 2022.Panel (a) shows that daily visits are particularly long in duration during the dry months of July-August, whereas panel (b) indicates that parrots land earlier during dry (June-August, January-March) than wet (specifically September-December, with insufficient data for April-May) season.Dots represent daily data, the smooth green lines denote trends derived from fitted generalized additive models (GAMs; light green = SE), and grey vertical columns indicate the rainy seasons.Bird and mammal species observed in the clearing of Ungwe in the Nkuba conservation area during the study period.Bird taxonomy followed(HBW and BirdLife International, 2022).